Enns returned to Westminster Theological Seminary in 1994 to begin his teaching career. He was tenured in 2000 and promoted to full professor in 2005 as Professor of Old Testament and Biblical Hermeneutics. Among other duties, he served as Associate Academic Dean from 1998 to 2001, chair of the Hermeneutics (Ph.D.) Field Committee (1997-2000), and edited the Westminster Theological Journal (2000-2005).[9]

Enns was a Senior Fellow, Biblical Studies with the BioLogos Foundation,[10] a Christian organization that "explores, promotes, and celebrates the integration of science and Christian faith".[11] He wrote nearly 100 blog posts at the BioLogos Forum, "Science and the Sacred." He also has written several pieces for the The Huffington Post's religion section.

Enns garnered significant attention for his 2005 book Inspiration and Incarnation: Evangelicals and the Problem of the Old Testament. His stated purpose for writing the book is “to bring an evangelical doctrine of Scripture into conversation with the implications generated by some important themes in modern biblical scholarship—particularly the Old Testament—over the past 150 years”.[15] Enns’s primary audience is those readers who find it difficult to maintain their faith in God because “familiar and conventional” evangelical approaches often mishandle the challenges raised by modern biblical scholarship.[16] Enns writes that evangelicals commonly take a defensive posture to new ideas, and that such defenses are “exercises in special pleading, attempts to hold on to comfortable idea despite evidence that makes such ideas problematic. It is precisely the ineffectiveness of certain ways of thinking about the Bible that can sometimes cause significant cognitive dissonance for Christians who love and want to hold on to their Bible, but who also feel the weight of certain kinds of evidence”[17]

Enns looks at three issues raised in modern biblical scholarship that he feels are mishandled by Evangelicals: (1) the strong similarities between the Old Testament and the literature of other ancient societies; (2), theological diversity among the Old Testament authors; (3) how New Testament writers interpreted the Old Testament in inventive ways that reflect Jewish practices of the time.[18]

In all three cases, the Bible behaves in ways that don’t seem very “inspired,” but rather very “human.” Enns argues for an “incarnational” understanding of the Bible as a way to take seriously these types of challenges. This model draws an analogy between Jesus and the Bible: “In the same way that Jesus is—must be—both God and human, the Bible is also a divine and human book”.[19] The Bible is not “an abstract, otherworldly book, dropped out of heaven. It was connected to and therefore spoke to those ancient cultures….precisely because Christianity is a historical religion, God’s word reflects the various historical moments in which Scripture was written”.[20] Enns feels that the problems raised by the “human dimension” of the Bible for many evangelicals “has less to do with the Bible itself and more to do with our own preconceptions” of how the Bible “ought” to be.[17] Enns advocates an incarnational model to help evangelicals reorient their expectations of Scripture and so come to peace with new developments in their understanding of the Bible.

Enns's book, Inspiration and Incarnation: Evangelicals and the Problem of the Old Testament, proved controversial at Westminster Theological Seminary (WTS). WTS President Peter Lillback expressed that it "has caught the attention of the world so that we have scholars that love this book, and scholars who have criticized it very deeply…. We have students who have read it say it has liberated them. We have other students that say it's crushing their faith and removing them from their hope. We have churches that are considering it, and two Presbyteries have said they will not send students to study under Professor Enns here."[21]

The general content of Inspiration and Incarnation was taught by Enns over his fourteen-year teaching career at Westminster Theological Seminary. It was only after the book’s publication in 2005 that a lengthy controversy ensued in the wake of major administrative changes, most notably the election of Peter Lillback as president in 2005. The main point of contention was whether the book was within the theological boundaries of the Westminster Confession of Faith. Westminster faculty members take an oath that their teaching will be in line with that confession.

Lillback initiated a series of regular faculty meetings ("Faculty Theology Fellowship") to discuss Enns and his book. Those meetings, moderated by Lillback, took place over a two-year period and led to the preparation of two written reports, at Lillback's direction, to aid the faculty in determining whether or not Enns was in violation of his oath. (It should be noted that, although Westminster has had a Board of Trustees for some time, it has historically been governed by its faculty, particularly in theological matters.) These reports were written by the two field committees: the Historical and Theological Field Committee, composed of faculty members generally opposed to Enns's book, and the Hermeneutics Field Committee, composed of members generally favorable towards Enns's ideas. After both committees reported their findings in the form of written reports, as well as written response by each committee to the other's report, faculty members William Edgar and Michael Kelly prepared a motion (known as the Edgar-Kelly Motion) declaring that Enns's writing and teaching were within the bounds of his faculty oath. All official documents used in these faculty debates, including both field committee reports and the Edgar-Kelly Motion, can be downloaded from the Westminster Theological Seminary web site here [1]. The motion was approved by the faculty, 12-8, in December 2007. Despite the work of these committees and the resulting faculty vote, President Lillback referred the matter immediately to the Board of Trustees.

On March 26, 2008, the Board of Trustees at Westminster Theological Seminary voted 18–9 to suspend Enns from his position effective May 23, 2008.[22] Though the faculty voted 12–8 that the work falls within the parameters of the Westminster Confession of Faith,[22] the chairman of the Board said that a majority of the members on the Board at that time felt the book was incompatible with the Confession.[21] As of August 1, 2008, Enns and the seminary agreed to part ways.[23] Following the Board's vote, nine trustees resigned from the board.

In September 2011, Enns's contract with BioLogos was not renewed. As of January 2012, Enns has been on the faculty of Eastern University (St. Davids, PA) teaching in the biblical studies department. In 2014 he was named Abram S. Clemens professor of biblical studies.